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AN EVOLUTIONARY SCENARIO FOR THE ORIGIN OF PENTARADIAL ECHINODERMS—IMPLICATIONS FROM THE HYDRAULIC PRINCIPLES OF FORM DETERMINATION Michael Gudo Morphisto-Evolutions-forschung und Anwendung GmbH, Senckenberganlage 25, 60325 Frankfurt am Main, Germany E-mail: [email protected] Received 27 May 2004; revised 4 December 2004, accepted 19 January 2005

ABSTRACT The early evolutionary history of echinoderms was reconstructed on the basis of structuralfunctional considerations and application of the quasi-engineering approach of ‘KonstruktionsMorphologie’. According to the presented evolutionary scenario, a bilaterally symmetrical ancestor, such as an enteropneust-like organism, became gradually modified into a pentaradial echinoderm by passing through an intermediate pterobranch-like stage. The arms of a pentaradial echinoderm are identified as hydraulic outgrowths from the central coelomic cavity of the bilateral ancestor which developed due to a shortening of the body in length but widening in the diameter. The resulting pentaradial symmetry is a consequence of mechanical laws that dictate minimal contact surface areas among hydraulic pneumatic entities. These developed in the coelomic cavity (metacoel) in the bilaterally symmetrical ancestor, when from the already U-shaped mesentery with the intestinal tract two additional U-shaped bows developed directly or subsequently. During the subsequent development tensile chords of the mesentery ‘sewed’ the gut with the body wall first in three and secondly in five ‘seams’. During the direct development five ‘seams’ between tensile chords and body wall developed straightly. These internal tensile chords subdivide the body coelom into five hydraulic subsystems (‘pneus’), which eventually arrange in a pentaradial pattern. The body could then enlarge only between the tensile chords, which means that five hydraulic bulges developed. These bulges initially supported the tentacles and finally each of them enclosed the tentacle until only the feather-like appendages of the tentacles projected over the surface. The tentacles with their feathers were transformed into the ambulacral system, and the bulges become the arms. These morphological transformations were accompanied and partly determined by specific histological modifications, such as the development of mutable connective tissues and skeletal elements that fused to ossicles and provided shape stabilization in form of a calcareous skeleton in the body wall. The organism resulted was an ancestral echinoderm (‘Ur-Echinoderm’) with an enlarged metacoel, stabilized by hydraulic pressure working against a capsule of mutable connective tissue, skeletal elements and longitudinal muscles. In regard to these reconstructions, the body structure of echinoderms can be understood as a hydraulic skeletal capsule.

Key Words: hydraulic principle, pentaradial echinoderms, engineering morphology, body construction, Echinodermata, Hemichordata, Bauplan, invertebrate evolution.

Acta Biotheoretica (2005) 53: 191–216

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Springer 2005

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1. INTRODUCTION The evolutionary origin and history of echinoderms is one of the least understood chapters of evolutionary history of metazoans and remains to be reconstructed in a satisfactory manner. Although echinoderm phylogeny was the topic of many authors, a satisfactory solution was not yet presented (for an overview see Gudo and Dettmann, 2005). While morphological and embryological investigations place the echinoderms in the ancestry of deuterostomes, recent molecular studies place the echinoderms close to the hemichordates and in a derived position (Furlong and Holland, 2002; Halanych, 1995; Peterson, 2004; Winchell et al., 2002) by re-introducing the term ‘Ambulacraria’ which was introduced by Metschnikoff (1881). Echinoderms are the only organisms that display a pentaradial symmetry of their body organization and their internal organs. This pentaradial arrangement develops ontogenetically from a bilaterally symmetrical larva through well-known growth and differentiation processes (David and Mooi, 1998; Hart, 2002; McCain and McClay, 1994; Morris, 1999; Wray, 1997). The evolutionary origin of the pentaradial organization, however, is less well understood. Several ideas have been presented to explain the pentaradial symmetry of echinoderms (David and Mooi, 1999; Hotchkiss, 1997; Jefferies, 1991; Kerr and Kim, 1999; McCain and McClay, 1994). Most of these authors argue about the efficiency and other advantages of the pentaradial organization of the tentacles of sea lilies, but do not describe an evolutionary process that could explain the evolutionary origin and biomechanical necessities of the pentaradial organization. Hotchkiss (1998) presented an overview over the seven schools of thought concerning the evolutionary origin of the pentaradial organisation. The ideas range from ‘highly adaptive’, ‘larval development’, ‘splitting of ambulacralia’ (two schools), ‘rays as appendages model’, ‘pentamerism as a primitive feature which is locked into echinoderms’ and ‘pentamerism as locked into development’. The proposed ideas of these schools of thought, however, do not provide an anagenetic reconstruction of the evolutionary processes that were likely to have been involved in the transformation from a bilateral to a pentaradial organism. They have used patterns of the skeletal capsule as characters for their phylogenetic reconstruction, but have not considered any structural-functional or physical-mechanical constraints that generally determine the major aspects of morphological transformations. Furthermore, nobody explained how a pentaradial body organization evolved from a non-echinoderm ancestor, it was only described how the pentaradial patterns of skeletal elements developed from non-pentaradial patterns from other echinoderms. Some authors argued that several non-pentaradial echinoderms display actually a primitive pentaradial organization, because their peristome is surrounded by five skeletal plates (for more details see Hotchkiss, 1998). However, this external character on a more or less spherical body is not necessarily indicative of a pentaradial body organization. It may be the result of physical constraints as it provides the most stable arrangement by minimizing the contact surfaces between the skeletal plates (Hargittai and Hargittai, 1996). Hence, the pentaradial arrangement of the skeletal plates surrounding the peristome may be the result of ‘fabricational noise’ (sensu Seilacher, 1973) and not a character that is useful for phylogenetic considerations. Since the skeletal capsule of echinoderms is produced by the soft tissue, a mechanically coherent explanation of the arrangement, shape and size of the skeletal plates needs to be prepared within the context of the entire organism and its constituent parts (Gutmann, 1991; Vogel, 1989a,

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1991a). This is also true for the pattern of sizes of the ambulacral basicoronal plates (i.e. Loven’s law, Lovén, 1874). Actually not a single explanation exists which shows how this pattern is related to mechanical necessities of the developing soft body. The fossil record of echinoderms does not reveal the relevant evolutionary transformations from a bilateral ancestor (Beaver et al., 1967a; Hyman, 1955). Already the earliest representatives of echinoderms are diverse and display a well-developed pentaradial organisation (Beaver et al., 1967a). Even the Lower Cambrian eocrinoids display brachioles that are arranged in groups of five. Even the most recent findings of early echinoderms raise more questions than they provide answers (Shu et al., 2004). Therefore, the evolutionary origin of echinoderms and their pentaradial body organization needs to be reconstructed by demonstrating how the pentaradial organization may have gradually evolved from a bilaterally symmetrical ancestor through known evolutionary mechanisms and biomechanical constraints. There is also the question of the evolutionary origin of the echinoderms as a group. The echinoderms have been considered as ancestors for the chordates (Eaton, 1970; Gislén, 1930; Jefferies et al., 1996), they have been derived from Sipunculids (Grobben, 1923; Nichols, 1962, 1967) or from certain larvae via paedomorphosis. The currently accepted model is the dipleurula model. It was originally proposed by Garstang (1894), and was presented by other authors in particular modifications (e.g., Jollie, 1962). In terms of morphological and embryological investigations it seems that every deuterostome and even some protostome animals have already been mentioned as ancestors for the echinoderms (for an overview see Gudo and Dettmann, 2005). Recently it was questioned whether the dipleurula theory would be a sufficient explanation for the evolutionary origin of echinoderms (Nezlin, 2000) and further molecular investigations of the 18S rDNA (Adoutte et al., 1999, 2000; Balavoine et al., 2002) provide new hypotheses concerning the anagenetic relationships between echinoderms and other deuterostomes (Cameron et al., 2000; Halanych, 1995; Peterson and Eernisse, 2001). Among the recent investigations, only Peterson et al. (2000) tried to integrate the larval bilateral symmetry with the adult pentaradial symmetry. He argued that the original anterior-posterior axis (A/P-axis) was preserved throughout the entire evolutionary pathway of the echinoderms, and that their arms and, therefore, the pentaradially symmetrical Bauplan of echinoderms developed by outgrowths of the central coelomic cavity of a bilateral, hemichordate-like ancestor. In support of their hypothesis, Peterson et al. (2000) pursued three lines of evidence: The expression patterns of a posterior class Hox gene in the coelom of the nascent adult larvae, the anatomy of certain early fossil echinoderms, and the relationship between the morphology of the endoskeletal plates and the associated coelomic tissues. All three lines of evidence lead to a single answer, namely that the anterior-posterior body axis extends from the mouth through the adult coelomic compartments and, consequently, there is but a single plane of symmetry dividing the echinoderm body into left and right halves. However, an anagenetic scenario reconstructing the sequence of morphological transformations that must have taken place during the evolutionary history of echinoderms is still needed. To do so, it is necessary to consider the functional design and the structuralfunctional and hydraulic principles constraining the body design, so that the morphological modifications from a bilateral ancestor into a pentaradial echinoderm can be reconstructed (Gutmann, 1988).

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2. THEORETICAL BACKGROUND By using the analytical approach of ‘Konstruktions-Morphologie’ (engineering morphology, constructional morphology, see Bock, 1991; Gudo, 2002; Gutmann, 1991; Vogel, 1991a) and by considering the hydraulic properties of body fluids as central shape-determining constraints (Clark, 1964; Gutmann, 1988), the animal body can be analysed in a manner similar to that used by an engineer to analyse the functioning of a technical apparatus with which he may be unfamiliar. Organisms are complex, dynamic, energy-transducing machines and hydraulic entities, and could not have evolved by a succession of chance events (Gutmann, 1991; Schmidt-Kittler and Vogel, 1991, 1989a). The hydraulic principle provides a crucial constraint for the determination of the shape of the body and its internal organs, because any fluid enclosed in a membrane behaves as a hydraulic entity (which is called a ‘pneu’ or ‘hydropneu’). Hence, hydraulic entities in living organisms are governed by mechanical laws that determine the interactions with one another and adjacent structures (Otto, 1977, 1978). Such hydraulic entities are not compressible and adjust their shape to surrounding structures and their mechanical forces. In summary, hydraulic entities in organisms are body elements that are integral for the functioning of the body, in particular for locomotion. Since fluid-filled cavities are omnipresent in organisms, and since internal organs, such as gonads or diverticles of the gut, can perform the functions of fluid-filled structures, organisms can be conceptualized as hydraulic entities (Gutmann, 1981, 1988). Another constraint that is useful for evolutionary reconstructions is provided by the fact that evolution proceeds as a seamless series of transformations of existing structures and not as a formation of new structures de novo. For reconstructions of evolutionary history, the recent representatives of a lineage need to be analysed first, because they provide insights into the functional design and biomechanical coherence of both the soft and hard body parts (Clark, 1964; Gutmann, 1988; Gutmann, 1991, 1993; Pantin, 1951). Subsequently a model of an organism summarizing only those structures which are structurally-functionally relevant can be constituted so that finally, the guiding principles for the reconstruction of evolutionary (anagenetic) scenarios can be named as structural-functional, biomechanical and hydraulic principles working as constraints of the evolutionary process (Bonik et al., 1977). Accordingly to these considerations, the reconstruction of the evolutionary history of echinoderms, comprises three major steps: (1) The conceptualisation of the ancestral echinoderm as an hydraulic entity; (2) the selection of a model organism of an echinoderm ancestor as a starting point for the morphological modifications; and (3) the reconstruction of the evolutionary history (i.e., anagenetic scenario) as a sequence of morphological modifications from an ancestral echinoderm to a recent one (including particular representatives from the fossil record).

3. THE FOSSIL RECORD AND IMPORTANT ANATOMICAL PRECONDITIONS The fossil record The fossil record does not provide direct evidence for an anagenetic scenario, because it usually does not reveal sufficient information about the early evolutionary steps of a lineage (Beaver et al., 1967a; Hyman, 1955). The fossil record shows only fossils that first


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have to be interpreted, reconstructed and conceptualized as organisms and secondly need to be integrated into an evolutionary scenario (Vogel, 1989b, 1991b; Vogel and Gutmann, 1988). However, only fossils can provide insight into the geological time scale during which particular evolutionary transformations have taken place. Furthermore, the fossil record can document bauplans (i.e., functional designs) that are not represented by recent organisms. The fossil record of echinoderms in the Spanish Cambrian-Ordovician sediments represents a good example of how fossils can be used for anagenetic reconstructions. Gil Cid et al. (2003) have shown that Eocrinoids in the Lower Cambrian were the earliest echinoderms, followed by Cincta and Cornuta in the Middle Cambrian, while Cystoids (i.e., Diploporita) occur not until the Ordovician. A biodiversification event during the Upper Ordovician can be inferred from the Spanish echinoderm fossils because at that point in time almost all recent groups of echinoderms are represented by various genera (Gil Cid et al., 2003). These results partly correspond to the global biostratigraphy of echinoderms. Although pentaradial echinoderms were known from the earliest echinoderm fossil record, the diversifications of echinoderms are first found in asymmetrical eocrinoids, subsequently in the asymmetrical homalozoans, followed by a diversification of triradiate echinoderms (e.g., the Helicoplacoidea), and concluded by an ‘event-like’ diversification within the pentaradial echinoderms. These observations provide crucial information aiding in the reconstruction of an anagenetic scenario of echinoderm evolution. On the one hand, pentaradial echinoderms existed from the very beginning of echinoderm evolution, but are not well represented in the fossil record. On the other hand, there is a sequence of diversification bursts proceeding from the asymmetrical echinoderms to the triradiate echinoderms and later to the pentaradial echinoderms. This raises the question whether these various echinoderm groups are anagenetically related to one another or whether they represent different evolutionary pathways. In any case, the fossil record documents that there are at least three functional designs (‘Körperkonstruktionen’) within the echinoderms, namely pentaradially and triradially symmetrical echinoderms and asymmetrical echinoderms. In addition, the fossil record reveals intermediate forms in which a pentaradial symmetry is superimposed on a triradiate symmetry. These observations suggest that more than one evolutionary pathway may have led from bilaterally symmetrical ancestors to the body plan of pentaradial echinoderms. At least one pathway may have been direct, at least another pathway may have been indirect by passing through a triradiate stage, and a third pathway may have led to asymmetrical or bilaterally symmetrical echinoderms.

The role of mutable connective tissues The mutable connective tissues play a crucial role in the functioning of the body of recent echinoderms. Histologically, these echinoderm connective tissues differ only slightly in their structure and properties from the collagenous connective tissues of vertebrates (Trotter et al., 2000, 1994). The main difference between the echinoderm and vertebrate connective tissues is that the former possess much more binding positions for proteoglucanes. These binding positions provide the echinoderm connective tissues with the capacity to stiffen and relax through neuronal stimulation and re-distribution of Ca2+ (Hill, 2001; Landeira-Fernandez, 2001), so that they can take on some functions

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that otherwise are performed by muscles. In holothurian echinoderms, for example, a stiffening of the mutable connective tissues generates a constant pressure on the liquid within the coelom. In recent isocrinoids, the mutable connective tissues can actively bend the trunk from side to side, and they can maintain a particular position of the stalk or arms for many hours to enable filter feeding (Erlinger et al., 1993; Welsch and Heinzeller, 1994). The similarities between the echinoderm and vertebrate connective tissues support the assumption that the echinoderm mutable connective tissues could have evolved from muscle tissues of a bilateral ancestor that was most likely related to chordates and their relatives (i.e., an ancestral deuterostome). The mechanical properties and physiological peculiarities of the echinoderm mutable connective tissues also throw some light on the origin of the rigid carbonate dermal skeleton of most echinoderms. That the stiffening of MCT is closely associated with the distribution of Ca2+ (Hill, 2001; Landeira-Fernandez, 2001) raises the possibility that under certain pH-conditions the Ca2+ could also react with CO3 2− to form CaCO3, so that calcareous spicules could grow in the tissues. Histological investigations indicate that the spicules are formed by a syncytial cell complex in which the carbonate is deposited between the syncytial membranes (i.e., in the endoplasmatic reticulum). During the growth of the spicules, the remaining cell plasma is continually reduced, so that finally the stereom structure resulted (Welsch and Heinzeller, 1994). The crystallisation of carbonate to a stereom might be supported by the stiffening of the body through its MCT. If the body wall were placed under constant pressure, crystals could grow and finally not only form spicules as in holothurians but also larger ossicles and bony plates as in sea urchins. Similar functional relationships between the carbonate structures in soft body tissues have been documented for several organisms (Vogel and Gutmann, 1981, 1988, 1989), and the importance of internal mechanical forces for tissue development has also been emphasized (Müller, 2003). The crucial mechanical role of mutable connective tissues is obvious in recent echinoderms. The permanent hydraulic pressure of the body fluids can be maintained only through the stiffening of the mutable connective tissue and would not feasible through a contraction of muscles. Muscles tend to fatigue and are energetically expensive to maintain. If in an evolutionary course additional spicules developed in the body wall of ancestral echinoderms, the eventual formation of a body wall with skeletal ossicles would have been initiated. Such an endoskeleton stabilizes the shape of the body and allows further increase in body size. This potential is related to the origin of mutable connective tissues and can be seen as a necessary precondition for the orgin of the echinoderms with their specific functional design.

4. RECONSTRUCTION OF THE EVOLUTIONARY HISTORY OF ECHINODERMS Conceptualisation of echinoderms as hydraulic entities The role of hydraulic shape-determining mechanisms during the growth of individuals were already described for sea urchins (Dafni, 1984, 1986, 1988; Johnson et al., 2002). Although Nachtigall (1996) has neglected the role of the hydraulic shape-determining mechanisms that are active in sea urchins, it has to be considered that every fluid filling which is enclosed by muscles, connective tissues and skeletal elements is under pressure


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and therefore acts as an hydraulic system and therefore provides specific constraints for functioning and for evolutionary transformations (Gutmann, 1985, 1988; Taylor and Kier, 2003). The ambulacral system of echinoderms is generally assumed to act as such an hydraulic system. As it can be observed in any living sea star or sea urchin, each podium is protruded when the hydraulic pressure in the ampullae increases through the contraction of ampullar muscles and it is retracted by longitudinal muscles in the wall of the tube. The fluid filled ambulacral system acts as a hydraulic skeleton and transmits the forces of the muscles. In the same manner, the fluid in the coelomic body cavity works as a hydraulic skeleton for the muscles of the body wall. In a sea star, the movements of the body are closely related to the force transmission via the fluid within the arms. Another obvious example of movements through hydraulic skeletons in echinoderms is the peristaltic movements of a sea cucumber in which the entire body fluid works as a force transmitter for the muscles and mutable connective tissues in the body wall during peristaltic movements (Haude, 1993, 2002). According to these observations, echinoderms have a body shape in which the coelomic fluid acts as a hydraulic skeleton and the body shape is generated and preserved by interactions between fluid-filled structures and the mutable connective tissues, thin muscles, and rigid carbonate skeletal elements. The muscles and the mutable connective tissues place the body fluid under pressure so that the arrangement of the tightening structures determines the body shape and its locomotory capacities (Figure 1, see also Gudo, 2004). This hydraulic conceptualisation is valid not only for the structural-functional complex of an individual and does not only determine its body shape (compare Clark, 1964), but with all surrounding anatomical structures it is a functional complex that constrains the frame of subsequent evolutionary changes and can therefore be used as a basis for the reconstruction of the evolutionary history (Gudo, 2002; Gutmann, 1972, 1988, 1993).

Selection of a precursor The selection of a precursor is necessary to have a starting point for the reconstruction of an evolutionary scenario. In this respect the work of Metschnikoff (1881) is of particular interest, because it already combines the enteropneusts, pterobranchs, and echinoderms into the Ambulacraria. Similar conclusions were drawn from recent molecular investigations in that the hemichordates (i.e., enteropneusts and pterobranchs) are a sister group of echinoderms (Balavoine and Adoutte, 2003; Bromham, 2003; Bromham and Degnan, 1999; Halanych, 1995; Janies, 2001; Lowe and Wray, 1997; Smith et al., 1993; Turbeville et al., 1994; Wada and Satoh, 1994) and in that the hemichordates and echinoderms together form the monophylum of Ambulacraria, which is placed next to the monophylum of chordates (Winchell et al., 2002). The anagenetic implications of these phylogenetic results are that an enteropneust-like organism may have given rise to the hemichordates on the one hand and to the echinoderms on the other hand (see also Peterson, 2004, 2000; Cameron, 2000). Neverthess, many other organisms have been discussed as precursors for echinoderms, but the most of them were not plausible in a structural-functional sense (Gudo and Dettmann, 2005). According to these results, recent hemichordates are eligible to point out those aspects of the functional design of the echinoderm ancestor which are relevant for the reconstruction.

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Figure 1. Hydraulic conceptualization of the echinoderm body structure. Echinoderms have a body structure in which the coelomic fluid (black) acts as a hydraulic skeleton enclosed in a endoskeletal capsule. The body shape is maintained through an interaction of the fluid-filled body cavities with the modifiable connective tissues, muscles (blue), and rigid calcified skeletal elements (white). The muscles and the modifiable connective tissues place the body fluids under pressure so that the arrangement of tightening structures determines the body shape and its locomotory capacities. Furtheron fibre networks and internal tensile chords constitute five hydraulic pneus—represented by the arms. Such pneus eventually arrange in a pentaradial pattern. Each of these arms carries a separate hydraulic system—the ambulacral system.


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Evolutionary origin and history of the echinoderms Evolutionary origin and functional design of the echinoderm ancestor An enteropneust-like ancestor is likely to have evolved from an ancestral chordate in which the notochord projected rostrally beyond the mouth opening (Gutmann and Bonik, 1979). Such organisms, which are similar to the recent Branchiostoma (Bonik and Gutmann, 1978; Gutmann, 1971), were able to attain a quasi-sessile life style by wriggling themselves into the sediment (Figure 2a). In the course of specific evolutionary transformations, the acranian-like body structure evolved into the body plan of an enteropneust-like organism. The most crucial steps in this transformation involved the re-arrangement of the muscle fibres of the front end of this organism. The muscles in the notochord region that projected beyond the mouth opening crossed over each other and formed a three-dimensional muscle network conteracting the enlarged fluid-filled cavity of the sclerocoels. Successively the front end developed a proboscis-like structure, capable of peristaltic movements, for improved burrowing actions (Figure 2b and 2c). Simultaneously the notochord was reduced completely and the longitudinal muscles of the trunk became thinner and thinner. From this evolutionary stage onwards, locomotion was no longer possible by lateral bending of the body. The hind end was transformed into a long fluid filled coelom cavity that contained only the intestinal tract. The remaining longitudinal muscles do not have an antagonistic muscle system. The circular muscles which are known from recent enteropneusts are not strong enough to be count as a noteworthy antagonistic system for efficient locomotory movements by the metasom. They only function as simple shape preserving structures. The longitudinal muscles were passively stretched when the animal moves through the sediment by peristaltic movements of the proboscis, and the metasome is pulled behind when subsequently the longitudinal muscles contract again (for more details see Gudo, in prep.-a; Gudo, in prep.-b; Gutmann and Bonik, 1979). The front end was transformed into a proboscis and a muscular collar surrounding the mouth (Figure 2b). Each of them—proboscis and collar—were hydromechanically separated from each other by a dissepiment so that they had their own hydraulic skeletons for their muscles. In the collar, also a part of the notochord remained as the so-called stomochord and proboscis skeleton, which both impart stabilization during peristaltic movements during burrowing (Gutmann, 1969, 1970, 1973; Gutmann and Bonik, 1979). However, the stomochord underwent particular modifications so that it histologically differs largely from the original notochord so that a relation between notochord and stomochord was discussed controversially (e.g. Mayer and Bartholomäeus, 2003; Newell, 1951; Takacs et al., 2002). Passage of a pterobranch-like intermediate From this enteropneust-like ancestor, the transformation to a pterobranch-like organism may have required only small changes, as a quasi sessile life-style can be attained by developing tentacles from the collar (Figure 2d). The use of tentacles allows a more effective and efficient feeding and, thereby, allows these organisms to conquer new environments. Under structural-functional aspects it appears as a process of economisation when in further transformations the hind opening of the gut was shifted to the front end, close to, but still outside of the tentacle crown. An enteropneust has to move its anus out of its tube defaecation, but any intermediate organism on this evolutionary course which

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Figure 2. Evolution of the echinoderm-ancestor. Early chordates (A) have only longitudinal muscles and a notochord as an internal force transmitter. They locomote by lateral bending of their body. As it can be observed in the recent lancelet, chordates with this body organization can also burrow in the sediment (a). If the notochord reaches over the mouth region, evolutionary modifications are possible, by which burrowing was improved and finally an enteropneust-like organism evolved (B). Hereby the notochord and the segmentation of the body were reduced and at the front end a proboscis capable for peristaltic movements developed. The hind end was elongated and contained the gut with gill slits and longitudinal muscles. The result was an organism with three body parts: proboscis, collar and metasome. Such an organism may attain a sessile life style (b, c) and it can be seen as an economization, when the gut attained an U-shaped course and when tentacles developed from the collar (C, d): the basic organization of a pterobranch-like ancestor. From this evolutionary stage the echinoderms evolved by further differentiations.

brings the anus into a rostral position could stay at its place for feeding and defaecation. This condition is still preserved in recent pterobranchs. Therefore, the intestinal tract attained a U-shaped configuration within the body (Figure 2c). The metasome now consisted of two parts, an anterior one with the gut and a very narrow posterior one containing body fluid. Basically the same muscle interaction as mentioned for enteropneusts can be observed in pterobranchs (Harrison and Ruppert, 1997). When a pterobranch creeps


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along a substrate or out of its capsule, the longitudinal muscles of the trunk are stretched; when the longitudinal muscles contract, they pull the body back. As in enteropneusts, the longitudinal muscles of these organisms have no noteworthy muscular antagonists. However, an agonistic-antagonstic relationship exists between these muscles and the proboscis (Bulman, 1955). This relationship is relevant for further evolutionary options, because it constrained the organisms to a the sessile life style. Origin of echinoderms and pterobranchs At this point of the evolutionary process, two evolutionary options are opened up, because the U-shaped configuration of the mesentery and intestinal tract could have been attained in different ways: (1) The U-shaped configuration could have been attained by shifting the anus in the mesenterium from caudal to rostral so that the gut and the mesenterium would be lying in the same plane. In that way the mesenterium would preserve its original dorso-ventral configuration and would be shifted from the rear end to the front end of the body along the dorsal line. This arrangement would lead to the condition found in the recent pterobranchs and most likely in the fossil graptoliths, as it enables the body to become smaller. It would even be possible that the mesentery could be entirely reduced. (2) The U-shaped configuration may have been attained by bending the gut together with its mesentery so that two sections of the gut and mesentery were to be situated in parallel in the dorso-ventral plane (Figure 3b).

Figure 3. Formation of the U-shaped gut in the pterobranch-like ancestor of echinoderms. A: The enteropneust-like ancestor shows a gut running along the entire organism. B: When the body enlarges in diameter and becomes thinner at the hindmost part, the gut is shifted into an U-shape until two layers of the mesentery are placed in the dorsoventral plane. During this transformation the coelomic cavities of the metacoel and protocoel are influenced. The right metacoel is succesively reduced while from the left metacoel tentacles develop. Bulging of the right metacoel supports the formation of a ring-like structure from the metacoel. Such an animal most likely lives in the sediment, only protruding the tentacles for collecting nutrition. However, the more the body is inflated, the more the body projects over the sediment which allows to gather nutrition from higher regions of the water column.

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According to this organization with internal tensile chords provided by the mesentery, the body cavity could enlarge in diameter. However, this widening of the body is only functional if mutable connective tissues and skeletal elements developed in the body wall (see above). Initially the enlargement could occur in the dorso-ventral plane, so that dorso-ventrally inflated, laterally compressed body shapes would result. This is the first stage from which several evolutionary pathways of non-pentaradial echinoderms may have differentiated, in particular representatives of the ‘homalozoan-pathways’ (such as stylophorans, ctenocystoids, homostelans, and homoiostelans, compare Gudo, 2005). It can be concluded that all echinoderms owe their existence to transformations that were initiated by an initial hydraulic inflation of the body wall, accompanied by a rearrangement of the intestinal tract with its mesentery providing internal tensile chords as tethering structures. To maintain the proper shape of the hydraulically inflated body the internal hydraulic pressure has to be maintained. In this context, the development of additional shape-stabilizing and pressure-generating anatomical structures can be seen as a necessary precondition and as part of a process of economisation (Vogel, 1979; Vogel and Gutmann, 1981, 1989). Such structures are the mutable connective tissues, the calcified skeletal elements, and additional internal tensile chords that counteract the expansion of the body fluids through osmosis. The questions that remain to be solved are: (1) How were the shape-determining structures arranged? (2) How do the shapedetermining structures interact with one another so that the organisms can maintain their non-spherical shapes, such as the ones of many recent and fossil echinoderms? And (3) how were these non-spherical shapes preserved during movements and individual growth? These questions can be at least partially answered through a model for the evolution of inflated body shapes. Evolution of inflated body shapes The body shape and the configuration of the gut were decisively affected when the body was inflated by internal fluid expansion. When this happened, the body was enlarged in its anterior part, whereas the hind part was narrowed and eventually transformed into a stalk and holdfast. The internal space of the anterior part became wider and shorter, as compared to the elongated shape of the ancestor. Accordingly, the intestinal tract had to be arranged in loops, unless it were dramatically shortened. However, the options of arranging the mesentery with the intestinal tract into loops are mechanically limited. One option is to create one additional loop, and the second option is to form two additional loops (compare Figure 4; everyone can test this by holding a belt at its two ends and then transforming the U-shaped form by help of another person). The particular transformation of the configuration of the mesentery influences the symmetry of the entire body shape, because the fibres of the mesentery were ‘sewed’ to the body wall in certain regions. If one additional loop is formed, the mesentery runs in 3 ‘seams’ along the body wall and if two additional loops developed the mesentery formed five ‘seams’ with the body wall (Figure 5). The arrangement of the mesentery and the looping of the gut are interdependent and are a consequence of the shortening of the body with a simultaneous increase in diameter. During an increase of a body’s diameter, the fibres of the mesentery act as tensile chords that hold the body wall in its place along the ‘seams’ (Figure 6(2)). However, the body wall would tend to bulge between the attachment


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points of the tensile chords because of the internal hydraulic pressure and continuing osmotic expansion (Figure 6(3)). These bulges are the hydraulic outgrowths of the central coelom as mentioned by Peterson (2000). They may grow, thereby initiating a radiate body organization that led eventually to a tri-radiate or penta-radiate pattern (Figures 6 and 7). The fossil record documents that both of these bauplans have actually existed (Beaver et al., 1967a, 1967b; Boardmann et al., 1987). Evolution of pentaradial echinoderms There are two possible evolutionary scenarios by which pentaradial echinoderms could have evolved: (1) Directly when five loops of the intestinal tract developed from the original U-shaped gut configuration; and (2) indirectly when the five loops of the intestinal tract developed from a three-looped configuration.

(A) Figure 4. The pentaradial organization of echinoderms evolved as consequence of the formation of loops of the intestinal tract. Originally the gut had a simple U-shape (A). When the body was shortened in its length, but enlarged in the diameter, the gut had to be laid in loops. The original bow of the intestinal tract first rotates about 90 deg and then forms two new U-shaped bows on each lateral side (B–D). The result are five regions in which the fibres of the mesentery are ‘sewed’ with the body wall. The body cavity was thereby subdivided into five portions, which work like five pneus in a physical sense; they push the five bulges into an exact pentaradial symmetrical pattern. This means that the distinct pentaradial symmetry of echinoderms evolved as a hydraulic necessity. (Continued on next page)

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(B)

(C) Figure 4. (Continued)


(D)

(E) Figure 4. (Continued)

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(F) Figure 4. (Continued)

Figure 5. The intestinal tract is ‘sewed’ by connective fibres of the mesentery to the body wall. These fibres provide internal tensile chords determining the body shape of the evolving echinoderm. Due to the loops of the intestinal tract, tensile chords reach the body wall in three or in five ‘seams’ whereas in the five large intervening regions tensile chords are absent. The figure here shows an evolutionary stage in which the second loop is in beginning of formation. The upper surface with the ambulacra is not shown.


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Figure 6. Direct evolution of pentaradial echinoderms. From the trunk (metasom) of the bilateral ancestor (1) with three body parts (proboscis, collar with tentacles, and metasome) hydraulic bulges grow out in five regions between the ‘seams’ of the mesentery fibres with the body wall (2, 3). These bulges support the tentacles which could become larger and finally countersunk into the dermal tissues (4). From each podium one end projected over the tissues to the outer medium and the other end projected over the tissues into the coelom of the arm and developed an ampulla. The tentacle crown was transformed into the ambulacral-system. The body shape which resulted could only be maintained unter permanent hydraulic pressure. This pressure was generated by mutable connective tissues and some muscles working together with many skeletal elements in the body wall against the internal fluid filling.

Direct evolution of the pentaradial organization In this direct evolutionary pathway towards a pentaradial organization, the U-shaped bow of the intestinal tract would first have been rotated about 90 deg, while the mouth and anus remained in their places. Next, two new U-shaped loops developed from the lower portion of the gut (Figure 4). As a consequence, the mesentery would have been connected to the body wall in five ‘seams’ (Figure 6(2)), while in the intervening five regions such tensile chords were absent. Accordingly the body cavity could hydraulically bulge out in those five regions without tethers. In a physical sense this organization can be described like five pneus which automatically attained an exact pentaradially symmetrical pattern (Figure 6(3)). This means that the distinct pentaradial symmetry of echinoderms evolved as a consequence of the rearrangement of the gut in the course of a shortening of the body.

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Figure 7. Indirect or subsequent evolution of pentaradial echinoderms. From the pterobranch-like ancestor (1) first only one internal loop developed so that fibres of the mesentery are ‘sewed’ to the body wall only in three ‘seams’. The result is a more or less voluminous, but triradial body shape (2). The tentacles countersunk into the body tissues and formed the ambulacral system (3). During further osmotic inflation of the body the gut formed an additional loop. The ambulacral system followed this transformation by splitting one ambulacral field into two branches so that an organism with four ambulacral fields resulted (4). Finally one of these branches splits again and five ambulacra were formed. The resulting organism shows a superimposition of the triraidal body symmetry by a pentaradial body symmetry (5).

If these outgrowths of the central coelom increased their size relatively rapidly in the course the subsequent evolution, they would attain an elongated shape (Figure 6(4)). This implies that they would have been slightly movable relative to one another. In this manner, the tentacles of the collar would have found a place to extend and to merge only on these outgrowths of the coelom, but not between them, where they would have been squashed. This might have been the reason for the uniform position of the ambulacralsystem on the five arms in recent pentaradial echinoderms irrespective of any variations in body shapes. In the compact forms, such as recent echinoids and holothurians or the fossil edrioasteroids, the arms became secondarily fused, but the former configuration of the arms remaining visible in the arrangement of the ambulacral fields.


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Indirect evolution of the pentaradial organization The structure of a number of fossil echinoderms suggests that primarily triradiate forms were subsequently modified into a pentaradial organization. Therefore, the scenario of an indirect evolution of the pentaradial arrangement is not only theoretical, but is correlated with particular findings in the fossil record (Hotchkiss, 1997, 1998). A first step in the transformation from a triradiate to a pentaradial organization was the evolutionary origin of a triradiate echinoderm as a consequence of the looping of the originally U-shaped gut into only one additional loop (Figure 7(2)). This configurational change of the gut would have resulted in the formation of a three-looped gut as a consequence of a shortening of the body. From these three loops, tensile chords would attach to the body wall along three ‘seams’. In the resulting triradiate body organisation only three tentacles of the collar were mechanically supported from the hydraulic bulges, so that eventually three ambulacral fields would have been formed (Figure 7(3)). From this triradiate body organization, which would have been generally voluminous and stout, certain triradiate echinoderms, such as the helicoplacoids and some hemicosmitids, are most likely to have evolved. The indirect-pentaradial echinoderms could now have evolved from an intermediate stage in which the body capsule was not yet completely stiffened by skeletal elements. In one of the three areas devoid of tensile chords, the looped gut would form an additional loop (Figure 7(4)) and a pentaradial symmetry would have been attained (Figure 7(5)). These evolutionary transitions would have given rise to a number of echinoderms that are known from the fossil record, including those that have four ambulacral fields (e.g., callocystids) and thereby represent intermediate forms. The ambulacral system The ambulacral system is probably the most conspicuous consequence of the development of the hydraulic outgrowth of the central coelom. In a worm-like ancestor, a tentacular crown had developed from the anterior margin of the collar. When the lateral bulges of the body projected more and more, they would have come into contact with the basal parts of tentacles. The tentacles could have grown along the bulges, providing a mechanical support, and finally the bulges pull the tentacles with them during further growth. The original tentacular crown cannot be reconstructed in detail, nor can it be established how many tentacles may have been present. However, a certain number of tentacles remained (e.g., five in the pentaradial forms), which were probably those that were mechanically supported by the bulges of the body wall and were histologically integrated in the inflated body parts. There are even some indications that the number of tentacles was also influenced by hydromechanical interactions of some metacoeloutpocketings with the mesocoel-sacs when they widen out into the region of the collar and enforced the origin of the ring-like structure of the ambulacral system. In fact, the former collar was more and more surrounded by the growing bulges of the body and did—relatively—sink into them so that nothing remained but a ring-canal where the tentacle canals start. In the course of evolution, the muscular proboscis of the ancestor has been entirely reduced, but its coelom, connected to the collar coelom and having an apical porus, remained. It formed the stone-canal and hydroporus of echinoderms, the only connection of the ring-canal to the open water. The final position of this hydropore may vary; probably it indicates that the mentioned evolutionary transformations have

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taken place several times, when similar body constructions show incompatible positions of the hydropore or anus. The tentacles fused more and more with the body wall of the hydraulic bulges, finally in their full length. Only the pinnules of the tentacle (=the ambulacral feet) running alternately along on both sides of the tentacle project over the surface. These pinnules can be individually moved and they can be protruded or retracted by fluid pressure when the ampullae at their bases had differentiated. These ampullae reach into the coelom of the trunk, while the radial canal itself remained in the body tissues. This assures a mechanically coherent organization and the possibility of the protrudable ends to develop ambulacral podia which can be used not only for particle catching but also for locomotion, as known from the recent eleutherozoa. In the indirect evolution of the pentaradial organization the ambulacral field of the segment in which the additional loop would have developed would have undergone particular transformations. One branch of the ambulacral field could have divided into two, and each new of these branches could have grown on the side where the new loop had formed, so that echinoderms with four ambulacral fields would have resulted (Figure 7(4)). If the curving of the intestinal tract and the rearrangement of mesenterial fibres is continued, one of the ambulacral fields would divide again, so that eventually each of the bulges would carry one ambulacral field (Figure 7(5)). The result would be echinoderms that display a pentaradial organization that is superimposed on a triradial organization. Echinoderms with such an organization are found in the rhombiferans. Many specimens within this group do not show the regular pentaradial organization that is typical, for example, for the eleutherozoans and edrioasteroids. Although the body shape that results from an indirect evolution of a pentaradial organization is superficially similar to the body shape that resulted from a direct evolution, there are, nevertheless, differences. Hence, two main evolutionary lineages have to be distinguished for the echinoderms beside the completely asymmetrical homalozoans. The recent echinoderms, and most likely also the edrioasteroids and blastoids, are part of the directly evolving pentaradial lineage, while many of the other fossil echinoderms are part of indirectly evolving pentaradial lineage.

5. CONCLUSION AND OUTLOOK The scenario that was presented in this study summarized the most important anagenetic modifications that were necessary to transform a bilaterally symmetrical organism into a pentaradially symmetrical echinoderm. However, reconstructing such scenarios is only one part of the work that is necessary for a complete understanding of the past evolutionary history, but it has to be the first part, because evolutionary scenarios cannot be reconstructed from the fossil record alone. On the one hand, there are too many gaps in the fossil record, and on the other hand, the phylogenetic as well as anagenetic relationships among fossils or recent organisms can only be inferred from theoretical considerations and reconstructions (Peters, 2002; Vogel, 1989b, 1991b). However, because basic hydromechanical and physical principles have been in the past as they are today, evolutionary modifications must have been constrained by the same natural laws that act on living recent organisms (Guntau, 1993). Therefore, an understanding of the functional design of recent organisms can be used as the basis for reconstructing the


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evolutionary changes that must have occurred in the past at the level of Bauplans (Gudo, 1997). The resulting reconstructions of anagenetic processes can subsequently be combined with the results of phylogenetic research. Phylogenetic trees always imply anagenetic relationships, but they do not explain or describe them. Anagenetic scenarios can be used to discuss phylogenetic trees by questioning their anagenetic implications (Huxley, 1957; Peters, 2002). This allows to decide whether a particular phylogenetic tree is plausible or whether it must be wrong, because it implies morphological transitions that are biomechanically impossible. Interestingly, the reconstructed scenario supports the hypothetical anagenetic implications from recent molecular investigations that suppose the Ambulacraria and Chordata as sistergroups within the Deuterostomia (e.g. Adoutte et al., 2000; Mallatt and Winchell, 2002; Winchell et al., 2002). Additionally the proposed scenario raises new questions for echinoderm research. For example, it may be possible to discover additional designs in the fossil record, which would have to be integrated into the present scenario. However, to answer this question fossil relics have to be interpreted with respect to their functional designs and not under morphological aspects only. Another remaining question would be how those echinoderms with more than five arms could have evolved. In most cases (e.g., the recent Solaster paposus and other sun-stars), the basic body configuration is pentaradially symmetrical, and additional arms developed by a subdivision of the original pentaradial body structure. A third aspect that has to be the topic of further research is an integration of the several thousands of fossil echinoderm species with the presented evolutionary scenario.

ACKNOWLEDGEMENTS I thank the DFG for funding the project GU566/1. Reimund Haude (Göttingen), Manfred Grasshoff (Frankfurt) read early and late versions of the manuscript. Tareq Syed (Frankfurt), Peter Jäger (Frankfurt), Dirk Kunz (Frankfurt) and Verena Schöning (Frankfurt) mentioned important aspects during discussions. Dominique G. Homberger (Baton Rouge) improved the language and has given helpfull comments for the final version of the manuscript. Antje Siebel-Stelzner prepared the illustrations. To all of them I extend my thanks.

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